Comparative analysis of the Saccharomyces cerevisiae and Caenorhabditis elegans protein interaction networks

BackgroundProtein interaction networks aim to summarize the complex interplay of proteins in an organism. Early studies suggested that the position of a protein in the network determines its evolutionary rate but there has been considerable disagreement as to what extent other factors, such as protein abundance, modify this reported dependence.ResultsWe compare the genomes of Saccharomyces cerevisiae and Caenorhabditis elegans with those of closely related species to elucidate the recent evolutionary history of their respective protein interaction networks. Interaction and expression data are studied in the light of a detailed phylogenetic analysis. The underlying network structure is incorporated explicitly into the statistical analysis. The increased phylogenetic resolution, paired with high-quality interaction data, allows us to resolve the way in which protein interaction network structure and abundance of proteins affect the evolutionary rate. We find that expression levels are better predictors of the evolutionary rate than a protein's connectivity. Detailed analysis of the two organisms also shows that the evolutionary rates of interacting proteins are not sufficiently similar to be mutually predictive.ConclusionIt appears that meaningful inferences about the evolution of protein interaction networks require comparative analysis of reasonably closely related species. The signature of protein evolution is shaped by a protein's abundance in the organism and its function and the biological process it is involved in. Its position in the interaction networks and its connectivity may modulate this but they appear to have only minor influence on a protein's evolutionary rate.

• Publication year

  2005

• Venue

  BMC Evolutionary Biology

• Publication date

  2005-03-03

• Fields of study

  Biology, Medicine, Physics

• Identifiers
  DOI 10.1186/1471-2148-5-23arXiv q-bio/0503008PMID 15777474PMCID 1079807
• External record

  Open on Semantic Scholar

• Source metadata

  Semantic Scholar, PubMed

• No claims are published for this paper.

• No concepts are published for this paper.

• Subnets of scale-free networks are not scale-free: sampling properties of networks.

  2005cited by this paper
• Clann: investigating phylogenetic information through supertree analyses

  2005cited by this paper
• Superfamilies of Evolved and Designed Networks

  2004cited by this paper
• Molecular Evolution in Large Genetic Networks: Does Connectivity Equal Constraint?

  2004cited by this paper
• Evidence for dynamically organized modularity in the yeast protein–protein interaction network

  2004cited by this paper
• Evolutionary rate depends on number of protein-protein interactions independently of gene expression level

  2004cited by this paper
• Gaining confidence in high-throughput protein interaction networks

  2004cited by this paper
• The Database of Interacting Proteins: 2004 update

  2004cited by this paper
• On the number of protein-protein interactions in the yeast proteome.

  2003cited by this paper
• Apparent dependence of protein evolutionary rate on number of interactions is linked to biases in protein–protein interactions data sets

  2003cited by this paper
• A simple dependence between protein evolution rate and the number of protein-protein interactions

  2003cited by this paper
• The Structure and Function of Complex Networks

  2003cited by this paper
• Selection on cost as a driver of molecular evolution.

  2003cited by this paper
• Correction: No simple dependence between protein evolution rate and the number of protein-protein interactions: only the most prolific interactors tend to evolve slowly

  2003influential reference
• Metabolic efficiency and amino acid composition in the proteomes of Escherichia coli and Bacillus subtilis

  2002cited by this paper
• Evolutionary Rate in the Protein Interaction Network

  2002influential reference
• Comparative assessment of large-scale data sets of protein–protein interactions

  2002cited by this paper
• Specificity and Stability in Topology of Protein Networks

  2002cited by this paper
• Statistical mechanics of complex networks

  2001cited by this paper
• The yeast protein interaction network evolves rapidly and contains few redundant duplicate genes.

  2001cited by this paper
• Highly expressed genes in yeast evolve slowly.

  2001cited by this paper
• DIP: The Database of Interacting Proteins: 2001 update

  2001cited by this paper
• The proteins of linked genes evolve at similar rates

  2000cited by this paper
• A genome-wide transcriptional analysis of the mitotic cell cycle.

  1998cited by this paper
• Molecular Evolution by Wen-Hsiung Li. Published by Sinauer Associates, Sunderland, MA, USA. ISBN: 0-87893-463-4 (cloth).

  1997cited by this paper
• An Introduction to the Bootstrap

  1995cited by this paper
• An Introduction to the Bootstrap CHAPMAN & HALL/CRC

  1993cited by this paper
• Mathematical Statistics and Data Analysis

  1988influential reference
• The codon Adaptation Index--a measure of directional synonymous codon usage bias, and its potential applications.

  1987cited by this paper
• STATISTICAL METHODS

  1967cited by this paper
• Statistical Methods

  1959influential reference
• Molecular Evolution

  year unknowncited by this paper

• A comprehensive review of global alignment of multiple biological networks: background, applications and open issues

  2022cites this paper
• America Addresses Two Epidemics: Cannabis and Coronavirus and their Interactions: An Ecological Geospatial Study

  2020cites this paper
• Position Matters: Network Centrality Considerably Impacts Rates of Protein Evolution in the Human Protein–Protein Interaction Network

  2017cites this paper
• An Improved Archaeology Algorithm Based on Integrated Multi-Source Biological Information for Yeast Protein Interaction Network

  2017cites this paper
• Genetic Variation of Goat Interferon Regulatory Factor 3 Gene and Its Implication in Goat Evolution

  2016cites this paper
• Coordinated Rates of Evolution between Interacting Plastid and Nuclear Genes in Geraniaceae

  2015cites this paper
• The reliability of the degree distribution of protein-protein interaction network in different species

  2015cites this paper
• Recent Positive Selection Has Acted on Genes Encoding Proteins with More Interactions within the Whole Human Interactome

  2015cites this paper
• The post-genomic era of biological network alignment

  2015cites this paper
• Molecular evolution constraints in the floral organ specification gene regulatory network module across 18 angiosperm genomes.

  2014cites this paper
• Inferring Functional Divergence in Protein Sequences

  2014cites this paper
• Detecting Functional Divergence after Gene Duplication through Evolutionary Changes in Posttranslational Regulatory Sequences

  2014cites this paper
• Reconstruction of phyletic trees by global alignment of multiple metabolic networks

  2013cites this paper
• Evolutionary characteristics of bacterial two-component systems.

  2012cites this paper
• The origins of the evolutionary signal used to predict protein-protein interactions

  2012influential citation
• Prediction of putative protein interactions through evolutionary analysis of osmotic stress response in the model yeast Saccharomyces cerevisae.

  2011cites this paper
• Evolutionarily stable and fragile modules of yeast biochemical network

  2011influential citation
• The Effects of Network Neighbours on Protein Evolution

  2011influential citation
• Integrative network alignment reveals large regions of global network similarity in yeast and human

  2011cites this paper
• Evidence for the additions of clustered interacting nodes during the evolution of protein interaction networks from network motifs

  2011cites this paper
• Predicting protein-protein interactions in the context of protein evolution.

  2010cites this paper
• Genome factor and gene pleiotropy hypotheses in protein evolution

  2010cites this paper
• Trees on networks: resolving statistical patterns of phylogenetic similarities among interacting proteins

  2010cites this paper
• Optimal Network Alignment with Graphlet Degree Vectors

  2010cites this paper
• The Evolution of the Phage Shock Protein Response System: Interplay between Protein Function, Genomic Organization, and System Function

  2010cites this paper
• Hypothesisfactor and gene pleiotropy hypotheses in protein evolution

  2010cites this paper
• Effect of protein thermostability on the cooperative function of split enzymes

  2010cites this paper
• An integrated view of molecular coevolution in protein-protein interactions.

  2010cites this paper
• The position of the RPL3 gene in a gene network relevant to diabetic microangiopathy

  2009cites this paper
• Progress in The Evolutionary Analysis of Protein Interaction Networks*: Progress in The Evolutionary Analysis of Protein Interaction Networks*

  2009cites this paper
• RETRACTED: Why proteins evolve at different rates: The functional hypothesis versus the mistranslation‐induced protein misfolding hypothesis

  2009cites this paper
• Evolution in protein interaction networks: co-evolution, rewiring and the role of duplication.

  2009cites this paper
• Molecular Evolution, Networks in

  2009cites this paper
• Chapter X Evolutionary Analyses of Protein Interaction Networks

  2009cites this paper
• Statistical Null Models for Biological Network Analysis

  2009cites this paper
• A Network Analysis Primer

  2009cites this paper
• Evolutionary Analyses of Protein Interaction Networks

  2009cites this paper
• The evolutionary consequences of erroneous protein synthesis

  2009cites this paper
• Topological network alignment uncovers biological function and phylogeny

  2008cites this paper
• Contact Density Affects Protein Evolutionary Rate from Bacteria to Animals

  2008cites this paper
• Protein-protein interactions: from global to local analyses.

  2008cites this paper
• Systems biology and its impact on anti-infective drug development.

  2007cites this paper
• Generating confidence intervals on biological networks

  2007influential citation
• Selection on Synthesis Cost Affects Interprotein Amino Acid Usage in All Three Domains of Life

  2007cites this paper
• Specificity in protein interactions and its relationship with sequence diversity and coevolution

  2007cites this paper
• Evolution at the system level: the natural history of protein interaction networks.

  2007influential citation
• A single determinant dominates the rate of yeast protein evolution.

  2006cites this paper
• A likelihood approach to analysis of network data

  2006cites this paper
• The effects of incomplete protein interaction data on structural and evolutionary inferences

  2006influential citation
• Structural determinants of the rate of protein evolution in yeast.

  2006cites this paper
• An integrated view of protein evolution

  2006cites this paper
• Sampling properties of random graphs: the degree distribution.

  2005cites this paper
• A single determinant for the rate of yeast protein evolution

  2005cites this paper
• Population Genetics of Translational Robustness

  2005cites this paper
• Current awareness on yeast

  2005cites this paper
• Complex networks and simple models in biology

  2005influential citation
• Statistical Model Selection Methods Applied to Biological Networks

  2005cites this paper
• Probability models for degree distributions of protein interaction networks

  2005cites this paper
• Networks in molecular evolution

  2002cites this paper